Development of the zebrafish myoseptum with emphasis on the myotendinous junction

Abstract

Zebrafish myosepta connect two adjacent muscle cells and transmit muscular forces to axial structures during swimming via the myotendinous junction (MTJ). The MTJ establishes transmembrane linkages system consisting of extracellular matrix molecules (ECM) surrounding the basement membrane, cytoskeletal elements anchored to sarcolema, and all intermediate proteins that link ECM to actin filaments. Using a series of zebrafish specimens aged between 24 h post-fertilization and 2 years old, the present paper describes at the transmission electron microscope level the development of extracellular and intracellular elements of the MTJ. The transverse myoseptum development starts during the segmentation period by deposition of sparse and loosely organized collagen fibrils. During the hatching period, a link between actin filaments and sarcolemma is established. The basal lamina underlining sarcolemma is well differentiated. Later, collagen fibrils display an orthogonal orientation and fibroblast-like cells invade the myoseptal stroma. A dense network of collagen fibrils is progressively formed that both anchor myoseptal fibroblasts and sarcolemmal basement membrane. The differentiation of a functional MTJ is achieved when sarcolemma interacts with both cytoskeletal filaments and extracellular components. This solid structural link between contractile apparatus and ECM leads to sarcolemma deformations resulting in the formation of regular invaginations, and allows force transmission during muscle contraction. This paper presents the first ultrastructural atlas of the zebrafish MTJ development, which represents an useful tool to analyse the mechanisms of the myotendinous system formation and their disruption in muscle disorders.

The development of zebrafish tendon and ligament progenitors

“…It has been demonstrated that the horizontal myosepta, which separate the epaxial and hypaxial musculature, are derived from the myotomal muscle pioneer cells (Devoto et al, 1996;Felsenfeld et al, 1991;Hatta et al, 1991;Schweitzer et al, 2005). By contrast, the vertical myosepta are believed to be of sclerotomal origin, making them analogous to mammalian axial tendon tissue (Bricard et al, 2014;Charvet et al, 2011). In the developing somite of zebrafish, which comprises predominantly myotomal cells, the sclerotomal cells form in the ventralmost domain and migrate dorsally to eventually surround the notochord and neural tube (Morin-Kensicki and Eisen, 1997; Stickney et al, 2000).…”

Tendon development and musculoskeletal assembly: emerging roles for the extracellular matrix

“…TPCs only appear later along the ISBs, where they contribute additional ECM to strengthen existing attachments in what we refer to here as a 'tendon-dependent' phase ( Fig. 3B) (Charvet et al, 2011Chen and Galloway, 2014;Subramanian and Schilling, 2014). Thus, in zebrafish, somitic muscles attach via the myomatrix at ISBs prior to the appearance of TPCs.…”

“…Studies of FACITs at zebrafish ISBs have been informative for understanding their functions as MTJs mature. In zebrafish, muscles first express Col12a1 and Col22a1 at larval stages and these progressively align into the orthogonal fibril arrays of mature MTJ/tendon ECM (Charvet et al, 2011. Col12a1 is expressed earlier than Col22a1 and colocalizes with Lama2 throughout muscle fiber attachment ).…”

CILP1 is dynamically expressed in the developing musculoskeletal system of the trout

“…Like tendons in amniotes, fish myosepta serve as transmitters of muscle contractility to bones. In the developing fish embryo, the myosepta are initially acellular and composed of matricial compounds such as fibronectin, laminin and collagens (Henry et al, 2005;Charvet et al, 2011;Bricard et al, 2014 ent in the intersomitic space (Charvet et al, 2011;Bricard et al, 2014;Chen and Galloway., 2014;Subramanian and Schilling., 2014). These myoseptal cells are considered homologous to axial tenocytes in amniotes: they express scleraxis, tenomodulin and tendon associated collagens (Bricard et al, 2014;Chen and Galloway, 2014) and, like axial tenocytes in amniotes (Brent et al, 2003), they probably originate from a somite-derived syndetome compartment (Bricard et al, 2014;Chen and Galloway, 2014;Subramanian and Schilling, 2014).…”

“…Like tendons in amniotes, fish myosepta serve as transmitters of muscle contractility to bones. In the developing fish embryo, the myosepta are initially acellular and composed of matricial compounds such as fibronectin, laminin and collagens (Henry et al, 2005;Charvet et al, 2011;Bricard et al, 2014). After somitogenesis, myoseptal cells become appar-ent in the intersomitic space (Charvet et al, 2011;Bricard et al, 2014;Chen and Galloway., 2014;Subramanian and Schilling., 2014).…”